Seasonally variable thermal performance curves prevent adverse effects of heatwaves
Intended for: GCB > Funct. Eco. > Proceedings B
Keywords: Heat wave, Copepod, Transgenerational, Plasticity, Seasonal,
Abstract
The increasing frequency and magnitude of heatwaves may represent a significant challenge for organisms in a changing climate beyond that posed by increasing mean temperatures. The direct impacts of heatwaves on populations depend on the relative position of environmental temperatures to the thermal performance curve optima. The effects of heatwaves may therefore vary seasonally along the annual temperature cycle. However, this seasonal variation may be dampened by corresponding variation in performance curves themselves. We investigate the effects of seasonal timing and duration on the impacts of heatwaves in the ecologically important copepod Acartia tonsa. We show that thermal performance curves are seasonally variable in the field, and that this variation buffers against negative effects of simulated heatwaves. Further, the offspring of individuals that experienced the simulated heatwave were raised in the laboratory to examine trans-generational effects of heatwaves on body size and reproductive output. The lack of a clear pattern in the trans-generational effects may indicate that seasonal variation in thermal performance curves also buffers against indirect effects of heat waves by reducing the effects of parental stress on the offspring. Our results show that seasonal variation in thermal performance curves has the potential to limit the adverse effects of heatwaves on marine copepods and other organisms with live spans shorter than the seasonal temperature cycle.
Introduction
- Heatwaves are increasing in both frequency and intensity. How do we define heatwaves? The acute nature of these events has large effects on organisms and need to be taken into account when predicting organismal responses to climate change.
- While past work has shown that heatwaves can have drastic effects on individual biology and population dynamics, and that the effects of heatwaves can vary across seasons, much of this is based on the perspective of fixed performance curves (i.e. - that the effect of heatwaves varies because the relative position of environmental temperature to TPC optimum varies). TPCs can be highly variable though, even over seasonal timescales. Variation in TPCs over seasonal timescales may act as a buffer against the negative effects of heatwaves on populations, as illustrated in the conceptual schematic below.
- Sources of variation in TPCs: 1) Genetic variation, balanced polymorphism fluctuating selection, etc. etc., 2) phenotypic plasticity.
- The effects of heat waves may also extend beyond direct effects on individuals; Transgenerational effects also need to be considered (maternal effects, transgenerational plasticity, etc.).
- Study / Methods summary statement
- Field experiments
- Simulated heatwave in laboratory
- Rearing of offspring in laboratory
- Hypothesis 1: TPCs of Acartia tonsa are seasonally variable not fixed.
- Hypothesis 2: For variable TPCs, the effects of heat waves will depend on the seasonal timing and duration of the event.
- Main findings statement
- TPCs are highly variable across seasons. This variation allows the population to maintain a relatively constant margin between field temperature and optimum temperature.
- There were generally no effects of heatwaves on the F0 individuals, and no pattern to the effects on the F1
- The mechanisms that produce seasonally variable TPCs, be they genetic or plastic, reduce the potential for heat waves to adversely affect population dynamics, and therefore increase resilience in the face of climate change.
Methods
Will need substantial input from other people to fill in the methods section.
Generating Field TPCs
Simulated Heat Waves
Transgenerational Experiments
Hypothesis Testing
Results
Seasonal Variation in TPCs
There was abundant variation in TPCs for Egg Production Rate (EPR), Hatching Success (HS), and production (the production of Hatching Success and Total Egg Production) for copepods collected throughout the year. EPR TPCs had higher optimum temperatures and maximum values in warmer months (July, August, and September) than in cooler months (October and November). Peaks were generally less distinct for HS than EPR. However, hatching success was generally higher in warmer months than cooler months, regardless of incubation temperature. When combined, the variation in optimum temperature and maximum value for EPR and HS curves yielded production curves that were highly variable. Collections from warmer months generally had slightly higher optimum temperatures as well as higher maximum fecundities. Thermal survivorship curves also varied significantly between collections.
Many of these traits tracked collection temperatures. Collection temperature never exceeded optimum temperatures, suggesting that at all times, additional warming (e.g. - a heatwave) would increase egg production. The one outlier was the second November collection, which was collected at 11 degrees C. This is around the threshold for resting egg production in A. tonsa. The extremely high estimated production optimum temperature may reflect the difference in hatching requirements between resting and subitaneous eggs. Thermal tolerance also increased with collection temperature, but this trend was not significant. The difference between environmental temperatures and thermal tolerance decreased as waters warmed. However, even during the warmest times, thermal tolerance values were always more than 8 degrees higher than water temperatures.
To summarize, there is a seasonally variable TPC for multiple traits in the Long Island Sound population of A. tonsa, keeping the optimum temperature and thermal tolerance values well above the environmental temperature. As a result, we’d predict heat waves should have a beneficial effect, regardless of seasonal timing, by moving the population towards its optimum temperature. However, strong heatwaves during the warmest times may have an adverse effect on survivorship, unless other mechanisms (e.g. - acclimation and phenotypic plasticity) adjust thermal tolerance.
Transgenerational Effects of Simulated Heatwave
F0 Individuals
The second component of this project examined the effects of heatwaves across generations. This necessarily began with reassessing the field collected F0. We examined the effects of short or long duration artificial heatwaves, during different collection months on EPR, HS, and production. We will focus the analysis on production, as it integrates the other traits. The ANOVA indicated no significant overall effect of heatwaves on production (p-value = 0.38). There was, however, a significant interaction between treatment and collection month (p-value = 0.01), indicating different effects of heatwaves across months. The different trial duration and collection months were also significantly different, with a significant interaction term as well. ANOVA results are shown in Supp. Table 1.
The effect sizes (the difference between heatwave and control trials, or between long and short duration trials) and confidence intervals were estimated using non-parametric bootstrap resampling. These estimates are shown below for the effects of treatment and the effect of duration. Short and long duration trials are shown in white and black symbols, respectively, in the first panel. The control and heatwave treatments are shown with different shapes in the second panel. Full Gardner-Altman estimation plots are shown in Supp. Fig 1 and 2. Effects of heatwaves were generally weak; only long heatwaves in June and short heatwaves in August had confidence intervals that did not (or nearly did not) overlap zero. In contrast, there were strong decreases in long duration trials relative to short trials, in both control and heatwave treatments.
F1 Individuals
We also examined the effects of parental exposure to heatwaves on offspring traits. Comparing between Control and Heatwave treatments now examines not the direct effects of increased temperature, but the indirect effect on offspring of parental exposure to heatwaves. In both panels, the gray boxes indicate the developmental temperature most similar to that experienced by offspring of the parental generation in the field.
Body Size - Offspring body size generally decreased with developmental temperature, as expected (Supp. Fig. 4). Within individual developmental temperatures, parental exposure to heatwaves also generally resulted in small decreases in body size. Short and long duration events are shown with open and filled circles respectively.
Fecundity - There were no consistent patterns in the effects of parental exposure to heatwaves across developmental temperatures, heatwave duration, or time of year.
General patterns…
…are scare in this data. Parental exposure to heat waves generally decreased offspring body size, but had no consistent effects on F1 production rates. Effects were particularly small when looking just at the developmental temperatures the offspring would experience in the field - At these temperatures, only parental exposure to heatwaves in August resulted in a decrease in offspring production or reduced body sizes.
The expectation is that production should decrease as body size decreases due to the effects on EPR. However, the changes in production were independent of changes in body size (Supp. Fig. 6). Instead, the observed effects are more likely to be the result of other mechanisms (such as maternal effects or transgenerational plasticity).
Supplemental Information
The ANOVA below shows the effects of duration, treatment, and collection month on production.
[1] “Production”
| Df | Sum Sq | Mean Sq | F value | Pr(>F) | |
|---|---|---|---|---|---|
| Day | 1 | 111469 | 111469 | 45.60 | 0.00 |
| Treatment | 1 | 1902 | 1902 | 0.78 | 0.38 |
| Month | 2 | 849627 | 424814 | 173.80 | 0.00 |
| Day:Treatment | 1 | 5549 | 5549 | 2.27 | 0.13 |
| Day:Month | 2 | 93553 | 46776 | 19.14 | 0.00 |
| Treatment:Month | 2 | 25657 | 12828 | 5.25 | 0.01 |
| Day:Treatment:Month | 2 | 4810 | 2405 | 0.98 | 0.37 |
| Residuals | 429 | 1048589 | 2444 | NA | NA |
These plots follow best practices for the visualization of differences between groups. The top half of each figure shows the underlying data points in a swarm plot. To the right of each each swarm is the mean and standard deviation of the group, represented using a gapped bar (gap = mean value). Below the raw data, the effect size and 95% confidence intervals are shown, which were obtained using non-parametric bootstrap resampling.
Here, the Gardner-Altman plot has been modified to show the repeated measures for each female using a Tufte slopegraph instead of a swarmplot. Production was generally lower in Days 5 to 7 than during days 1 to 3, regardless of treatment (heat wave vs. control), although not for all collections (production increased in the longer trials in November) - However, note the y-axis scale for the female responses relative to those from the other months. A similar decrease in both control and heatwave treatments might suggest effects of aging on female reproductive output. A stronger decrease in the heatwave treatment than in the control, might indicate cumulative effects of the increased temperature. An increase in production over time might be expected from the effects of beneficial acclimation.
The effects of parental heatwave exposure varied strongly between collections, heatwave duration, and offspring temperature. As a reminder, these represent carry-over effects of heat waves - differences observed here do not represent the direct effects of heat waves, but rather indirect effects of parental exposure to heat waves. In June, Short heatwaves increased production relative to controls at intermediate offspring temperatures, while long heat waves decreased production relative to controls. In August, short heat waves had very little effect on production, while long heat waves generally decreased production. In November, both long and short heatwaves had positive effects on production at intermediate temperatures. Short heatwaves also increased production at high offspring temperatures relative to the control.
